Patient-specific structural connectivity informs outcomes of responsive neurostimulation for temporal lobe epilepsy
Chantel M. Charlebois
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Scientific Computing & Imaging Institute, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorDaria Nesterovich Anderson
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Department of Pharmacology & Toxicology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorKara A. Johnson
Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida, USA
Department of Neurology, University of Florida, Gainesville, Florida, USA
Search for more papers by this authorBrian J. Philip
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorTyler S. Davis
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorBlake J. Newman
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAngela Y. Peters
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAmir M. Arain
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAlan D. Dorval
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorJohn D. Rolston
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Scientific Computing & Imaging Institute, University of Utah, Salt Lake City, Utah, USA
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorCorresponding Author
Christopher R. Butson
Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida, USA
Department of Neurology, University of Florida, Gainesville, Florida, USA
Department of Neurosurgery, University of Florida, Gainesville, Florida, USA
Department of Biomedical Engineering, University of Florida, Gainesville, Florida, USA
Correspondence
Christopher R. Butson, Fixel Institute, University of Florida, Gainesville, FL, USA.
Email: [email protected]
Search for more papers by this authorChantel M. Charlebois
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Scientific Computing & Imaging Institute, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorDaria Nesterovich Anderson
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Department of Pharmacology & Toxicology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorKara A. Johnson
Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida, USA
Department of Neurology, University of Florida, Gainesville, Florida, USA
Search for more papers by this authorBrian J. Philip
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorTyler S. Davis
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorBlake J. Newman
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAngela Y. Peters
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAmir M. Arain
Department of Neurology, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorAlan D. Dorval
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorJohn D. Rolston
Department of Biomedical Engineering, University of Utah, Salt Lake City, Utah, USA
Scientific Computing & Imaging Institute, University of Utah, Salt Lake City, Utah, USA
Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorCorresponding Author
Christopher R. Butson
Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida, USA
Department of Neurology, University of Florida, Gainesville, Florida, USA
Department of Neurosurgery, University of Florida, Gainesville, Florida, USA
Department of Biomedical Engineering, University of Florida, Gainesville, Florida, USA
Correspondence
Christopher R. Butson, Fixel Institute, University of Florida, Gainesville, FL, USA.
Email: [email protected]
Search for more papers by this authorAbstract
Objective
Responsive neurostimulation is an effective therapy for patients with refractory mesial temporal lobe epilepsy. However, clinical outcomes are variable, few patients become seizure-free, and the optimal stimulation location is currently undefined. The aim of this study was to quantify responsive neurostimulation in the mesial temporal lobe, identify stimulation-dependent networks associated with seizure reduction, and determine if stimulation location or stimulation-dependent networks inform outcomes.
Methods
We modeled patient-specific volumes of tissue activated and created probabilistic stimulation maps of local regions of stimulation across a retrospective cohort of 22 patients with mesial temporal lobe epilepsy. We then mapped the network stimulation effects by seeding tractography from the volume of tissue activated with both patient-specific and normative diffusion-weighted imaging. We identified networks associated with seizure reduction across patients using the patient-specific tractography maps and then predicted seizure reduction across the cohort.
Results
Patient-specific stimulation-dependent connectivity was correlated with responsive neurostimulation effectiveness after cross-validation (p = .03); however, normative connectivity derived from healthy subjects was not (p = .44). Increased connectivity from the volume of tissue activated to the medial prefrontal cortex, cingulate cortex, and precuneus was associated with greater seizure reduction.
Significance
Overall, our results suggest that the therapeutic effect of responsive neurostimulation may be mediated by specific networks connected to the volume of tissue activated. In addition, patient-specific tractography was required to identify structural networks correlated with outcomes. It is therefore likely that altered connectivity in patients with epilepsy may be associated with the therapeutic effect and that utilizing patient-specific imaging could be important for future studies. The structural networks identified here may be utilized to target stimulation in the mesial temporal lobe and to improve seizure reduction for patients treated with responsive neurostimulation.
CONFLICT OF INTEREST
AMA has served as a consultant for NeuroPace. JDR has served as a consultant for Medtronic, NeuroPace, and Corlieve Therapeutics. CRB has recently served as a consultant for NeuraModix and Abbott and holds intellectual property related to neuromodulation therapy. The remaining authors have no conflicts of interest.
Supporting Information
| Filename | Description |
|---|---|
| epi17298-sup-0001-TableS1.docxWord 2007 document , 19.8 KB |
Table S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Morrell MJ. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011; 77: 1295–304. https://doi.org/10.1212/WNL.0b013e3182302056
- 2Heck CN, King-Stephens D, Massey AD, Nair DR, Jobst BC, Barkley GL, et al. Two-year seizure reduction in adults with medically intractable partial onset epilepsy treated with responsive neurostimulation: Final results of the RNS System Pivotal trial. Epilepsia. 2014; 55: 432–41. https://doi.org/10.1111/epi.12534
- 3Bergey GK, Morrell MJ, Mizrahi EM, Goldman A, King-Stephens D, Nair D, et al. Long-term treatment with responsive brain stimulation in adults with refractory partial seizures. Neurology. 2015; 84: 810–7. https://doi.org/10.1212/WNL.0000000000001280
- 4Nair DR, Laxer KD, Weber PB, Murro AM, Park YD, Barkley GL, et al. Nine-year prospective efficacy and safety of brain-responsive neurostimulation for focal epilepsy. Neurology. 2020; 95(9): e1244–56. https://doi.org/10.1212/WNL.0000000000010154
- 5Razavi B, Rao VR, Lin C, Bujarski KA, Patra SE, Burdette DE, et al. Real-world experience with direct brain-responsive neurostimulation for focal onset seizures. Epilepsia. 2020; 61(8): 1749–57. https://doi.org/10.1111/epi.16593
- 6Geller EB, Skarpaas TL, Gross RE, Goodman RR, Barkley GL, Bazil CW, et al. Brain-responsive neurostimulation in patients with medically intractable mesial temporal lobe epilepsy. Epilepsia. 2017; 58: 994–1004. https://doi.org/10.1111/epi.13740
- 7Jobst BC, Kapur R, Barkley GL, Bazil CW, Berg MJ, Bergey GK, et al. Brain-responsive neurostimulation in patients with medically intractable seizures arising from eloquent and other neocortical areas. Epilepsia. 2017; 58: 1005–14. https://doi.org/10.1111/epi.13739
- 8Ma BB, Fields MC, Knowlton RC, Chang EF, Szaflarski JP, Marcuse LV, et al. Responsive neurostimulation for regional neocortical epilepsy. Epilepsia. 2019; 61: 96–106. https://doi.org/10.1111/epi.16409
- 9 RNS® System Programming Manual, 2021 [cited 2022 Feb 04]. Availabile from: https://www.neuropace.com/wp-content/uploads/2021/02/neuropace-rns-system-programming-manual.pdf
- 10Scheid BH, Bernabei JM, Khambhati AN, Mouchtaris S, Jeschke J, Bassett DS, et al. Intracranial electroencephalographic biomarker predicts effective responsive neurostimulation for epilepsy prior to treatment. Epilepsia. 2022; 63: 652–62. https://doi.org/10.1111/epi.17163
- 11Chiang S, Khambhati AN, Wang ET, Vannucci M, Chang EF, Rao VR. Evidence of state-dependence in the effectiveness of responsive neurostimulation for seizure modulation. Brain Stimul. 2021; 14: 366–75. https://doi.org/10.1016/j.brs.2021.01.023
- 12Khambhati AN, Shafi A, Rao VR, Chang EF. Long-term brain network reorganization predicts responsive neurostimulation outcomes for focal epilepsy. Sci Transl Med. 2021; 13(608):eabf6588. https://doi.org/10.1126/scitranslmed.abf6588
- 13Kokkinos V, Sisterson ND, Wozny TA, Richardson RM. Association of Closed-Loop Brain Stimulation Neurophysiological Features with Seizure Control among Patients with Focal Epilepsy. JAMA Neurol. 2019; 76: 800. https://doi.org/10.1001/jamaneurol.2019.0658
- 14Sander JWAS, Hart YM, Shorvon SD, Johnson AL. MEDICAL SCIENCE. National General practice study of epilepsy: newly diagnosed epileptic seizures in a general population. Lancet. 1990; 336: 1267–71. https://doi.org/10.1016/0140-6736(90)92959-L
- 15Téllez-Zenteno JF, Hernández-Ronquillo L. A review of the epidemiology of temporal lobe epilepsy. Epilepsy Res Treat. 2012; 2012: 1–5. https://doi.org/10.1155/2012/630853
10.1155/2012/630853 Google Scholar
- 16Bondallaz P, Boëx C, Rossetti AO, Foletti G, Spinelli L, Vulliemoz S, et al. Electrode location and clinical outcome in hippocampal electrical stimulation for mesial temporal lobe epilepsy. Seizure. 2013; 22(5): 390–5. https://doi.org/10.1016/J.SEIZURE.2013.02.007
- 17Wozny C. Comment on “On the origin of interictal activity in human temporal lobe epilepsy in vitro”. Science. 2003; 80: 301–463. https://doi.org/10.1126/science.1084237
10.1126/science.1084237 Google Scholar
- 18Jo HJ, Kenny-Jung DL, Balzekas I, Benarroch EE, Jones DT, Brinkmann BH, et al. Nuclei-specific thalamic connectivity predicts seizure frequency in drug-resistant medial temporal lobe epilepsy. NeuroImage Clin. 2019; 21:101671. https://doi.org/10.1016/j.nicl.2019.101671
- 19Travers RF. Limbic epilepsy. J R Soc Med. 1991; 84: 454–6. https://doi.org/10.1177/014107689108400804
- 20Blumenfeld H. Impaired consciousness in epilepsy. Lancet Neurol. 2012; 11: 814–26. https://doi.org/10.1016/S1474-4422(12)70188-6
- 21Jefferys JGR, Jiruska P, de Curtis M, Avoli M. Limbic network synchronization and temporal lobe epilepsy. In: J Noebels, M Avoli, M Rogawski, R Olsen, A Delgado-Escueta, editors. Jasper's basic mechanisms of the epilepsies. Oxford: Oxford University Press; 2013. https://doi.org/10.1093/med/9780199746545.003.0014
- 22Bernhardt BC, Bernasconi N, Kim H, Bernasconi A. Mapping thalamocortical network pathology in temporal lobe epilepsy. Neurology. 2012; 78(2): 129–36. https://doi.org/10.1212/WNL.0b013e31823efd0d
- 23Larivière S, Weng Y, Vos de Wael R, Royer J, Frauscher B, Wang Z, et al. Functional connectome contractions in temporal lobe epilepsy: Microstructural underpinnings and predictors of surgical outcome. Epilepsia. 2020; 61(6): 1221–33. https://doi.org/10.1111/epi.16540
- 24McDonald CR, Hagler DJJ, Ahmadi ME, Tecoma E, Iragui V, Gharapetian L, et al. Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia. 2008; 49(5): 794–803. https://doi.org/10.1111/j.1528-1167.2008.01539.x
- 25Liu M, Bernhardt BC, Hong S-J, Caldairou B, Bernasconi A, Bernasconi N. The superficial white matter in temporal lobe epilepsy: a key link between structural and functional network disruptions. Brain. 2016; 139(Pt 9): 2431–40. https://doi.org/10.1093/brain/aww167
- 26Bernhardt BC, Bernasconi A, Liu M, Hong SJ, Caldairou B, Goubran M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol. 2016; 80(1): 142–53. https://doi.org/10.1002/ana.24691
- 27Morgan VL, Johnson GW, Cai LY, Landman BA, Schilling KG, Englot DJ, et al. MRI network progression in mesial temporal lobe epilepsy related to healthy brain architecture. Netw Neurosci. 2021; 5(2): 434–50. https://doi.org/10.1162/netn_a_00184
- 28Rossi MA, Stebbins G, Murphy C, Greene D, Brinker S, Sarcu D, et al. Predicting white matter targets for direct neurostimulation therapy. Epilepsy Res. 2010; 91: 176–86. https://doi.org/10.1016/j.eplepsyres.2010.07.010
- 29Davis TS, Caston RM, Philip B, Charlebois CM, Anderson DN, Weaver KE, et al. LeGUI: A fast and accurate graphical user interface for automated detection and anatomical localization of intracranial electrodes. Front Neurosci. 2021; 15: 1693.
- 30Thielscher A, Antunes A, Saturnino GB. Field modeling for transcranial magnetic stimulation: a useful tool to understand the physiological effects of TMS? In: Proceedings of the annual international conference of the IEEE Engineering in Medicine and Biology Society, EMBS. New York City, NY:IEEE (Institute for Electrical and Electronics Engineers); 2015. Volume 2015, p. 222–5. https://doi.org/10.1109/EMBC.2015.7318340
10.1109/EMBC.2015.7318340 Google Scholar
- 31Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008; 12: 26–41. https://doi.org/10.1016/j.media.2007.06.004
- 32Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012; 62(2): 782–90. https://doi.org/10.1016/j.neuroimage.2011.09.015
- 33Chen DQ, Dell'Acqua F, Rokem A, et al. Diffusion weighted image co-registration: investigation of best practices. bioRxiv. 2019;864108. https://doi.org/10.1101/864108
10.1101/864108 Google Scholar
- 34Dell'Acqua F, Lacerda LM, Catani M, Simmons A. Anisotropic power maps: a diffusion contrast to reveal low anisotropy tissues from HARDI data. Proc Intl Soc Mag Reson Med. 2014; 22: 29960–7.
- 35Butson CR, Cooper SE, Henderson JM, McIntyre CC. Patient-specific analysis of the volume of tissue activated during deep brain stimulation. Neuroimage. 2007; 34(2): 661–70. https://doi.org/10.1016/j.neuroimage.2006.09.034
- 36Howell B, McIntyre CC. Analyzing the tradeoff between electrical complexity and accuracy in patient-specific computational models of deep brain stimulation. J Neural Eng. 2016; 13:36023. https://doi.org/10.1088/1741-2560/13/3/036023
- 37Malaga KA, Costello JT, Chou KL, Patil PG. Atlas-independent, N-of-1 tissue activation modeling to map optimal regions of subthalamic deep brain stimulation for Parkinson disease. NeuroImage Clin. 2021; 29:102518. https://doi.org/10.1016/j.nicl.2020.102518
- 38Si H. TetGen, a delaunay-based quality tetrahedral mesh generator. ACM Trans Math Softw. 2015; 41: 1–36. https://doi.org/10.1145/2629697
- 39Akhtari M, Bryant HC, Mamelak AN, Flynn ER, Heller L, Shih JJ, et al. Conductivities of three-layer live human skull. Brain Topogr. 2002; 14(3): 151–67. https://doi.org/10.1023/a:1014590923185
- 40Baumann SB, Wozny DR, Kelly SK, Meno FM. The electrical conductivity of human cerebrospinal fluid at body temperature. IEEE Trans Biomed Eng. 1997; 44: 220–3. https://doi.org/10.1109/10.554770
- 41Anderson DN, Osting B, Vorwerk J, Dorval AD, Butson CR. Optimized programming algorithm for cylindrical and directional deep brain stimulation electrodes. J Neural Eng. 2018; 15: 26005. https://doi.org/10.1088/1741-2552/aaa14b
- 42Wei XF, Grill WM. Current density distributions, field distributions and impedance analysis of segmented deep brain stimulation electrodes. J Neural Eng. 2005; 2: 139–47. https://doi.org/10.1088/1741-2560/2/4/010
- 43Zhang TC, Grill WM. Modeling deep brain stimulation: Point source approximation versus realistic representation of the electrode. J Neural Eng. 2010; 7(6):66009. https://doi.org/10.1088/1741-2560/7/6/066009
- 44Rattay F. Analysis of Models for External Stimulation of Axons. IEEE Trans Biomed Eng. 1986; 33(10): 974–7. https://doi.org/10.1109/TBME.1986.325670
- 45Duffley G, Anderson DN, Vorwerk J, Dorval AD, Butson CR. Evaluation of methodologies for computing the deep brain stimulation volume of tissue activated. J Neural Eng. 2019; 16: 66024. https://doi.org/10.1088/1741-2552/ab3c95
- 46Anderson DN, Duffley G, Vorwerk J, Dorval AD, Butson CR. Anodic stimulation misunderstood: Preferential activation of fiber orientations with anodic waveforms in deep brain stimulation. J Neural Eng. 2019; 16: 16026. https://doi.org/10.1088/1741-2552/aae590
- 47Butson CR, Cooper SE, Henderson JM, Wolgamuth B, McIntyre CC. Probabilistic analysis of activation volumes generated during deep brain stimulation. Neuroimage. 2011; 54: 2096–104. https://doi.org/10.1016/j.neuroimage.2010.10.059
- 48Johnson KA, Fletcher PT, Servello D, Bona A, Porta M, Ostrem JL, et al. Image-based analysis and long-term clinical outcomes of deep brain stimulation for Tourette syndrome: A multisite study. J Neurol Neurosurg Psychiatry. 2019; 90: 1078–90. https://doi.org/10.1136/jnnp-2019-320379
- 49Cooper SE, Driesslein KG, Noecker AM, McIntyre CC, Machado AM, Butson CR. Anatomical targets associated with abrupt versus gradual washout of subthalamic deep brain stimulation effects on bradykinesia. PLoS One. 2014; 9(8):e99663. https://doi.org/10.1371/journal.pone.0099663
- 50Reich MM, Horn A, Lange F, Roothans J, Paschen S, Runge J, et al. Probabilistic mapping of the antidystonic effect of pallidal neurostimulation: a multicentre imaging study. Brain. 2019; 142(5): 1386–98. https://doi.org/10.1093/brain/awz046
- 51Wang Q, Akram H, Muthuraman M, Gonzalez-Escamilla G, Sheth SA, Oxenford S, et al. Normative vs. patient-specific brain connectivity in deep brain stimulation. Neuroimage. 2021; 224:117307. https://doi.org/10.1016/j.neuroimage.2020.117307
- 52Horn A, Reich M, Vorwerk J, Li N, Wenzel G, Fang Q, et al. Connectivity Predicts deep brain stimulation outcome in Parkinson disease. Ann Neurol. 2017; 82: 67–78. https://doi.org/10.1002/ana.24974
- 53Johnson KA, Duffley G, Anderson DN, Ostrem JL, Welter ML, Baldermann JC, et al. Structural connectivity predicts clinical outcomes of deep brain stimulation for Tourette syndrome. Brain. 2020; 143: 2607–23. https://doi.org/10.1093/brain/awaa188
- 54Baldermann JC, Melzer C, Zapf A, Kohl S, Timmermann L, Tittgemeyer M, et al. Connectivity profile predictive of effective deep brain stimulation in obsessive-compulsive disorder. Biol Psychiatr. 2019; 85: 735–43. https://doi.org/10.1016/j.biopsych.2018.12.019
- 55Al-Fatly B, Ewert S, Kübler D, Kroneberg D, Horn A, Kühn AA. Connectivity profile of thalamic deep brain stimulation to effectively treat essential tremor. Brain. 2019; 142(10): 3086–98. https://doi.org/10.1093/brain/awz236
- 56Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K. The WU-Minn Human Connectome Project: an overview. Neuroimage. 2013; 80: 62–79. https://doi.org/10.1016/j.neuroimage.2013.05.041
- 57Riva-Posse P, Choi KS, Holtzheimer PE, McIntyre CC, Gross RE, Chaturvedi A, et al. Defining critical white matter pathways mediating successful subcallosal cingulate deep brain stimulation for treatment-resistant depression. Biol Psychiatry. 2014; 76(12): 963–9. https://doi.org/10.1016/j.biopsych.2014.03.029
- 58Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. Abingdon: Routledge; 1988. https://doi.org/10.4324/9780203771587
10.1046/j.1526-4610.2001.111006343.x Google Scholar
- 59Fan L, Li H, Zhuo J, Zhang Y, Wang J, Chen L, et al. The Human brainnetome atlas: a new brain atlas based on connectional architecture. Cereb Cortex. 2016; 26(8): 3508–26. https://doi.org/10.1093/cercor/bhw157
- 60Klein A, Tourville J. 101 labeled brain images and a consistent human cortical labeling protocol. Front Neurosci. 2012; 6: 171. https://doi.org/10.3389/fnins.2012.00171
- 61Tavakol S, Royer J, Lowe AJ, Bonilha L, Tracy JI, Jackson GD, et al. Neuroimaging and connectomics of drug-resistant epilepsy at multiple scales: from focal lesions to macroscale networks. Epilepsia. 2019; 60(4): 593–604. https://doi.org/10.1111/epi.14688
- 62Gleichgerrcht E, Kocher M, Bonilha L. Connectomics and graph theory analyses: Novel insights into network abnormalities in epilepsy. Epilepsia. 2015; 56(11): 1660–8. https://doi.org/10.1111/epi.13133
- 63Jo HJ, Kenney-Jung DL, Balzekas I, Welker KM, Jones DT, Croarkin PE, et al. Relationship between seizure frequency and functional abnormalities in limbic network of medial temporal lobe epilepsy. Front Neurol. 2019; 10: 1–8. https://doi.org/10.3389/fneur.2019.00488
- 64Middlebrooks EH, Grewal SS, Stead M, Lundstrom BN, Worrell GA, Van Gompel JJ. Differences in functional connectivity profiles as a predictor of response to anterior thalamic nucleus deep brain stimulation for epilepsy: a hypothesis for the mechanism of action and a potential biomarker for outcomes. Neurosurg Focus. 2018; 45: E7. https://doi.org/10.3171/2018.5.focus18151
- 65Morgan VL, Englot DJ, Rogers BP, Landman BA, Cakir A, Abou-Khalil BW, et al. Magnetic resonance imaging connectivity for the prediction of seizure outcome in temporal lobe epilepsy. Epilepsia. 2017; 58(7): 1251–60. https://doi.org/10.1111/epi.13762
- 66Morgan VL, Rogers BP, González HFJ, Goodale SE, Englot DJ. Characterization of postsurgical functional connectivity changes in temporal lobe epilepsy. J Neurosurg. 2019; 133: 1–11. https://doi.org/10.3171/2019.3.JNS19350
- 67Ezama L, Hernández-Cabrera JA, Seoane S, Pereda E, Janssen N. Functional connectivity of the hippocampus and its subfields in resting-state networks. Eur J Neurosci. 2021; 53(10): 3378–93. https://doi.org/10.1111/ejn.15213
- 68Nunna RS, Borghei A, Brahimaj BC, Lynn F, Garibay-Pulido D, Byrne RW, et al. Responsive neurostimulation of the mesial temporal white matter in bilateral temporal lobe epilepsy. Neurosurgery. 2021; 88(2): 261–7. https://doi.org/10.1093/neuros/nyaa381
- 69Bharath RD, Sinha S, Panda R, Raghavendra K, George L, Chaitanya G, et al. Seizure frequency can alter brain connectivity: evidence from resting-state fMRI. Am J Neuroradiol. 2015; 36(10): 1890–8. https://doi.org/10.3174/ajnr.A4373
- 70Quigg M, Skarpaas TL, Spencer DC, Fountain NB, Jarosiewicz B, Morrell MJ. Electrocorticographic events from long-term ambulatory brain recordings can potentially supplement seizure diaries. Epilepsy Res. 2020; 161:106302. https://doi.org/10.1016/j.eplepsyres.2020.106302
- 71Hoppe C, Poepel A, Elger CE. Epilepsy: Accuracy of patient seizure counts. Arch Neurol. 2007; 64:1595. https://doi.org/10.1001/archneur.64.11.1595
- 72Kerling F, Mueller S, Pauli E, Stefan H. When do patients forget their seizures? An electroclinical study. Epilepsy Behav. 2006; 9(2): 281–5. https://doi.org/10.1016/j.yebeh.2006.05.010
- 73Gregg NM, Marks VS, Sladky V, Lundstrom BN, Klassen B, Messina SA, et al. Anterior nucleus of the thalamus seizure detection in ambulatory humans. Epilepsia. 2021; 62: e158–64. https://doi.org/10.1111/epi.17047
- 74Cendejas Zaragoza L, Byrne RW, Rossi MA. Pre-implant modeling of depth lead placement in white matter for maximizing the extent of cortical activation during direct neurostimulation therapy. Neurol Res. 2017; 39: 198–211. https://doi.org/10.1080/01616412.2016.1266429
- 75Peña E, Zhang S, Deyo S, Xiao Y, Johnson MD. Particle swarm optimization for programming deep brain stimulation arrays. J Neural Eng. 2017; 14(1): 16014. https://doi.org/10.1088/1741-2552/aa52d1
- 76Adkinson JA, Tsolaki E, Sheth SA, Metzger BA, Robinson ME, Oswalt D, et al. Imaging versus electrographic connectivity in human mood-related fronto-temporal networks. Brain Stimul. 2022; 15(3): 554–65. https://doi.org/10.1016/j.brs.2022.03.002
- 77Wang YC, Kremen V, Brinkmann BH, Middlebrooks EH, Lundstrom BN, Grewal SS, et al. Probing circuit of Papez with stimulation of anterior nucleus of the thalamus and hippocampal evoked potentials. Epilepsy Res. 2019; 2020(159):106248. https://doi.org/10.1016/j.eplepsyres.2019.106248
- 78Silva AB, Khambhati AN, Speidel BA, Chang EF, Rao VR. Effects of anterior thalamic nuclei stimulation on hippocampal activity: chronic recording in a patient with drug-resistant focal epilepsy. Epilepsy Behav Reports. 2021; 16:100467. https://doi.org/10.1016/j.ebr.2021.100467
- 79Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010; 51(5): 899–908. https://doi.org/10.1111/j.1528-1167.2010.02536.x
- 80Velasco F, Velasco M, Jiménez F, Velasco AL, Brito F, Rise M, et al. Predictors in the treatment of difficult-to-control seizures by electrical stimulation of the centromedian thalamic nucleus. Neurosurgery. 2000; 47(2): 295–305. https://doi.org/10.1097/00006123-200008000-00007
- 81Cooper IS, Amin I, Riklan M, Waltz JM, Poon TP. Chronic cerebellar stimulation in epilepsy. Clinical and anatomical studies. Arch Neurol. 1976; 33(8): 559–70. https://doi.org/10.1001/archneur.1976.00500080037006
- 82Velasco F, Carrillo-Ruiz JD, Brito F, Velasco M, Velasco AL, Marquez I, et al. Double-blind, randomized controlled pilot study of bilateral cerebellar stimulation for treatment of intractable motor seizures. Epilepsia. 2005; 46(7): 1071–81. https://doi.org/10.1111/j.1528-1167.2005.70504.x
- 83Boutet A, Madhavan R, Elias GJB, Joel SE, Gramer R, Ranjan M, et al. Predicting optimal deep brain stimulation parameters for Parkinson's disease using functional MRI and machine learning. Nat Commun. 2021; 12(1): 3043. https://doi.org/10.1038/s41467-021-23311-9
Citing Literature
